Bert Hölldobler

The number of queens: An important trait in ant evolution

The pervasive social and ecological differences between ant colonies that have a single queen and those that have multiple queens are defined. The evolutionary tendencies which lead to polygyny and the adaptive significance of multiple queens are examined. The discussion of the ecological consequences of polygyny and monogyny leads to a deeper understanding of territoriality, spacing and species packing in ants.

Recruitment behavior, home range orientation and territoriality in harvester ants, Pogonomyrmex

Summary1.Scouts of the harvester ant Pogonomyrmex barbatus, P. maricopa and P. rugosus which discovered a new rich foraging area recruit nestmates by laying a trail with poison gland contents from the feeding site to the nest. Laboratory experiments have shown that Pogonomyrmex workers are stimulated to follow the trail by the trail pheromone alone.2.The biological significance of the recruitment behavior was analyzed in the mesquite-acacia desert in Arizona-New Mexico, where the three species occur sympatrically. P. maricopa recruits less efficiently to food sources than does P. barbatus and P. rugosus. Generally the recruitment activity depends on a number of parameters of the food source, such as distance to the nest, density of the seed fall and size of the grains.3.The recruitment activity is also affected by the presence, absence or distance of hostile neighboring colonies.4.The use of chemically and visually marked trunk trails which originate from recruitment trails, guarantees and efficient partitioning of foraging grounds. It could be demonstrated that trunk trails, used by P. barbatus and P. rugosus during foraging and homing, have the effect of avoiding aggressive confrontations between neighboring colonies of the same species. They channel the mass of foragers of hostile neighboring nests into diverging directions, before each ant pursues its individual foraging exploration. This channeling subtly partitions the foraging grounds and allows a much denser nest spacing pattern than a foraging strategy without trunk trails, such as that employed by P. maricopa.5.The behavioral mechanisms which maintain overdispersion both within and between species of Pogonomyrmex were investigated. Aggressive confrontations at the colony level and aggressive expulsion of foundress queens from the nest territories of mature colonies play thereby a major role. Observational as well as experimental data led to the conclusion that the farther away from its nest the intruder is, the less vigorous are the aggressive confrontations with the defenders. Only when neighboring colonies are located too close together will increased aggressive interactions eventually lead to the emigration of the weaker colony.6.P. barbatus and P. rugosus have a wide niche overlap, whereas P. maricopa seems to be more specialized in regard to food. This is consistent with the findings that interspecific territoriality between P. barbatus and P. rugosus is considerably more developed than between these species on the one side and P. maricopa on the other.7.Although foundress queens, which venture into a territory of a conspecific mature colony are fiercely attacked, most of them are not injured, but rather dragged or carried to the territorial border and then released.8.Nevertheless foraging areas, even of conspecific colonies, frequently overlap, but aggressive interactions there are usually less intense than at the core areas (trunk trails plus nest yards), which normally do not overlap and are vigorously defended.

The genome sequence of Blochmannia floridanus: Comparative analysis of reduced genomes

Bacterial symbioses are widespread among insects, probably being one of the key factors of their evolutionary success. We present the complete genome sequence of Blochmannia floridanus, the primary endosymbiont of carpenter ants. Although these ants feed on a complex diet, this symbiosis very likely has a nutritional basis: Blochmannia is able to supply nitrogen and sulfur compounds to the host while it takes advantage of the host metabolic machinery. Remarkably, these bacteria lack all known genes involved in replication initiation (dnaA, priA, and recA). The phylogenetic analysis of a set of conserved protein-coding genes shows that Bl. floridanus is phylogenetically related to Buchnera aphidicola and Wigglesworthia glossinidia, the other endosymbiotic bacteria whose complete genomes have been sequenced so far. Comparative analysis of the five known genomes from insect endosymbiotic bacteria reveals they share only 313 genes, a number that may be close to the minimum gene set necessary to sustain endosymbiotic life.

The kin recognition system of carpenter ants (Camponotus spp.) - I. Hierarchical cues in small colonies

SummaryThe phenotypic cues that provide for rejection of non-nestmates by workers of the ant genus Camponotus could derive from any or all of four sources: (1) environmental odors; (2) the individuals own genetically-determined recognition pheromones or “discriminators”; (3) a “gestalt” or mixture of transferable discriminators, produced by each nestmate and absorbed by all; and/or (4) the discriminators of the queen applied to all nestmates. To test these hypotheses, four series of small experimental colonies were created: inter- and intraspecific mixed colonies containing queens, queenless worker groups, and pairs of worker groups between which a single queen was repeatedly switched. Intraspecific mixed colonies and queenless groups were further divided into groups receiving different diets. Aggression of workers in 165 experimental colonies was assayed in a total of 4064 neutral arena tests. Workers adopted into inter- and intraspecific mixed colonies with queens were highly aggressive to unfamiliar kin from pure colonies, independent of diet and of the proportion of different kin groups in the colony. However, queenless workers exhibited less aggression to unfamiliar kin than to non-kin, demonstrating the existence of worker discriminators. Diet differences slightly enhanced aggression among unfamiliar queenless kin. Non-kin sharing a switched queen were as unaggressive to one another as were sisters. The ability to adopt queenless workers between colonies gradually declined over 1–2 wks following their emergence from pupae. We propose a hierarchy of importance of cue sources in determining nestmate discrimination in small Camponotus colonies: Queen discriminators> worker discriminators>environmental cues. A flow-diagram model of social insect kin recognition, based on the “phenotype matching” concept of Holmes and Sherman (1983), is discussed.

The multiple recruitment systems of the african weaver ant Oecophylla longinoda (Latreille) (Hymenoptera: Formicidae)

Summary1.African weaver ants (Oecophylla longinoda) utilize no less than five recruitment systems to draw nestmates from the leaf nests to the remainder of the nest tree and to the foraging areas beyond: (a) recruitment to new food sources, mediated by odor trails produced from the rectal gland, a newly discovered exocrine organ, together with tactile stimuli presented during mouth-opening, antennation, and head-waggling; (b) recruitment to new terrain, entailing odor trails released from the rectal gland and tactile stimulation through antennation: (c) emigration to new sites; (d) short-range recruitment to territorial intruders, during which the terminal abdominal sternite is maximally exposed and dragged for short distances over the ground to release an attractant from the sternal gland, a second newly discovered structure; and (e) long-range recruitment to intruders, mediated by odor trails from the rectal gland and by antennation and intense body jerking.These systems exist in addition to the elaborate pheromone-mediated alarm communication previously described by Bradshaw et al. (1975). In aggregate, the alarm and recruitment systems of O. longinoda constitute the most complex of such repertories thus far discovered in ants.2.Weaver ants recognize new terrain by means of both visual and olfactory cues, with the latter being the more effective. When major workers cannot cross gaps to the terrain by walking, they attempt to make the traverse by building bridges with their bodies. Individuals are attracted to the bridge site visually, but when the bridge is complete, they recruit nestmates to the new terrain with rectal-gland odor trails.3.Workers mark newly acquired home range with randomly placed drops of fluid extruded from the rectal vesicle. They distinguish their own domain from that of alien conspecific colonies in part by means of the odor of the anal spots. When a section of terrain is found unmarked, the rate of anal-drop deposition is accelerated, even when adjacent areas are already heavily marked.4.The anal substance is a true territorial pheromone: workers respond to alien spots initially with hostility and aversion, then by recruiting nestmates to the vicinity. In laboratory experiments, workers entering an arena simultaneously with workers from alien colonies always gained the initial advantage in the ensuing conflict if they had previously been allowed to mark the arena. When the arena was placed in a spatial position familiar to one colony but possessed a floor previously marked by the second colony, the second colony still won. To our knowledge these results represent the first demonstration of a true territorial pheromone in the social insects.5.During foraging the Oecophylla workers move independently of one another and are distributed at random (Poisson distributed) or with slight temporary clumping of no more than two or three workers. Short-range recruitment of intruders causes the ants to shift to a more distinctly clumped pattern, involving as many as ten or more workers, at the same time that long-range recruitment brings more defenders into the vicinity. Together the two forms of response result in a more efficient capture of intruders that are too large to be immobilized by only one or two workers.6.The complex recruitment and territorial behavior displayed by O. longinoda is considered to be part of the adaptation of these relatively large ants to a strongly arboreal existence. The similarity of four of the recruitment systems to each other (1 a, b, c, and e above) is interpreted as an example of signal economy in the evolution of social insect communication systems. The parallel evolution has been enhanced by the lack of any strong functional distinction between territorial defense and predation (see Discussion).6.Signal ritualization appears to have occurred in at least two contexts: the modification of body thrusting during territorial battles into the jerking signal used in long-range recruitment of nestmates to enemies; and the adoption of anal excrement in the chemical marking of territories.

The kin recognition system of carpenter ants (Camponotus spp.). II: Larger colonies

SummaryPrevious investigations of small colonies (<10 workers each) of Camponotus spp. indicated that queen-derived recognition cues, transferred to and learned by workers, are of major importance in between-colony discrimination (Carlin and Hölldobler 1983, 1986). However, queens may have contributed disproportionately to a communal label or “gestalt” in small colonies. Here we report experiments on groups of approximately 190 sister workers of C. floridanus, adopted to alien conspecific queens. In 1200 neutral arena encounters, adoptees were introduced to their own unfamiliar sisters, reared in their colony of origin; unfamiliar non-sisters were introduced as controls. Following tests of worker behavior, the queens were dissected. Aggression was equally strong in encounters between unfamiliar kin and encounters between nonkin, if the adoptive queen had fully-developed ovaries, was completely inseminated, and produced abundant brood. However, workers were significantly less aggressive in encounters between kin if their queens had less active ovaries and were incompletely inseminated. Thus the presence of a fully functional queen continues to prevent recognition of unfamiliar kin in larger colonies, but worker cues can become more important when the queen is ineffective. In addition, adoptees of productive queens were significantly less aggressive toward pure-colony sisters than the latter were to them, suggesting the involvement of a foreignlabel rejection mechanism (Getz 1982).

Cuticular hydrocarbons mediate discrimination of reproductives and nonreproductives in the ant Myrmecia gulosa

In many species of social insects, the cuticular hydrocarbons of adults vary with both colony identity and individual physiology (oogenesis). Such variations have been shown in some ants and social wasps to function in nestmate recognition, but as yet there is no demonstration of their use by workers to recognize egg layers. We report that in the ant Myrmecia gulosa, workers can discriminate queens and fertile workers from infertile individuals based on distinctive blends of long-chained hydrocarbons present both on the cuticle and in the postpharyngeal gland. The purified hydrocarbon fraction of cuticular extracts from queens elicited high interest in workers, unlike the nonhydrocarbon fraction. However, both fractions were necessary to trigger a response of maximal intensity. In contrast, extracts of mandibular and Dufour glands from queens or infertile workers were not treated differentially by workers. We suggest that cuticular hydrocarbons function as pheromones allowing for recognition of the queen as well as egg-laying workers.

Colony founding in Myrmecocystus mimicus wheeler (Hymenoptera: Formicidae) and the evolution of foundress associations

Summary1.Field studies of the honey ant Myrmecocystus mimicus have revealed that colonies are often founded by groups of foundresses ranging in size from 2–9 females, with groups of 2–4 females being most common. Founding nests are also aggregated together in patches which are distant from existing M. minicus colonies.2.Laboratory experiments have shown that colony founding involves inter-colony raiding: the brood from neighboring incipient colonies is transported by workers from one nest to another. Ultimately all of the brood ends up in a single nest chamber which the workers adopt as their own. Workers frequently abandon their mothers in favor of these nests. We conclude that competition among founding nests favors foundress associations and that inter-colony raiding is a natural consequence of aggregated pleometrotic founding nests.3.A general theory of the evolution of foundress associations is developed which describes the conditions under which foundress associations will be favored. It is shown that the evolution of foundress groups of particular sizes depends on the shape of the colony productivity function. Increasing relatedness among foundresses will generally result in a larger optimum foundress group size. Production data on foundress groups of different sizes gathered in the laboratory on M. mimicus are analyzed using the theory developed. It is shown that the size of foundress associations expected on the basis of the theory is very near the value observed in nature.

Recruitment and food-retrieving behavior in Novomessor (Formicidae, Hymenoptera) - I. Chemical signals

Summary1Novomessor cockerelli and N. albisetosus have been considered by previous authors to be individual foragers. This investigation, however, has demonstrated that workers of both species employ recruitment techniques when they encounter large prey.2.Novomessor workers usually carry large food items in a cooperative action directly to the nest.3.The chemical communication system employed during foraging was investigated in laboratory and field experiments. Secretions released from the poison gland proved to be the most effective recruitment signal.4.In order to summon nestmates to large food objects, Novomessor employs the following two different recruitment techniques.Short-range recruitment: After discovering the prey, the scout releases poison gland secretion into the air. Nestmates already in the vicinity are attracted from as far away as 2 m and move upwind toward the prey.Long-range recruitment: If short-range recruitment does not attract enough foragers, a scout lays a chemical trail with poison gland secretion from the prey to the nest. Nestmates are stimulated by the pheromone alone to leave the nest and follow the trail toward the prey.5.The trail pheromone is short-lived, and trail laying consequently does not lead to mass communication. Instead, the pheromone releases a short pulse of outrushing ants, usually numerous enough to subdue the prey and to carry it home when the ants act jointly.In several field experiments, we demonstrated that these recruitment and prey-retrieving techniques enable Novomessor to counteract interference competition by mass-recruiting ant species.

Biomechanics of the movable pretarsal adhesive organ in ants and bees

Hymenoptera attach to smooth surfaces with a flexible pad, the arolium, between the claws. Here we investigate its movement in Asian weaver ants (Oecophylla smaragdina) and honeybees (Apis mellifera).  When ants run upside down on a smooth surface, the arolium is unfolded and folded back with each step. Its extension is strictly coupled with the retraction of the claws. Experimental pull on the claw-flexor tendon revealed that the claw-flexor muscle not only retracts the claws, but also moves the arolium. The elicited arolium movement comprises (i) about a 90° rotation (extension) mediated by the interaction of the two rigid pretarsal sclerites arcus and manubrium and (ii) a lateral expansion and increase in volume. In severed legs of O. smaragdina ants, an increase in hemolymph pressure of 15 kPa was sufficient to inflate the arolium to its full size. Apart from being actively extended, an arolium in contact also can unfold passively when the leg is subject to a pull toward the body.  We propose a combined mechanical–hydraulic model for arolium movement: (i) the arolium is engaged by the action of the unguitractor, which mechanically extends the arolium; (ii) compression of the arolium gland reservoir pumps liquid into the arolium; (iii) arolia partly in contact with the surface are unfolded passively when the legs are pulled toward the body; and (iv) the arolium deflates and moves back to its default position by elastic recoil of the cuticle.